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Archaeal Proviruses TKV4 and MVV Extend the PRD1-Adenovirus Lineage to the Phylum Euryarchaeota ⁎ Mart Krupovič, Dennis H

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Archaeal Proviruses TKV4 and MVV Extend the PRD1-Adenovirus Lineage to the Phylum Euryarchaeota ⁎ Mart Krupovič, Dennis H CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Available online at www.sciencedirect.com Virology 375 (2008) 292–300 www.elsevier.com/locate/yviro Archaeal proviruses TKV4 and MVV extend the PRD1-adenovirus lineage to the phylum Euryarchaeota ⁎ Mart Krupovič, Dennis H. Bamford Department of Biological and Environmental Sciences, Biocenter 2, P.O. Box 56 (Viikinkaari 5), FIN-00014 University of Helsinki, Finland Institute of Biotechnology, Biocenter 2, P.O. Box 56 (Viikinkaari 5), FIN-00014 University of Helsinki, Finland Received 17 December 2007; returned to author for revision 28 January 2008; accepted 30 January 2008 Available online 4 March 2008 Abstract The viral lineage hypothesis predicting a common origin for viruses that infect hosts residing in different domains of life gains more support as data on viral structures accumulates. One such lineage is the PRD1-adenovirus lineage, which unites icosahedral dsDNAviruses with large facets and a double β-barrel trimer coat protein. This lineage is represented by a number of viruses infecting bacteria and eukaryotes. However, only one member of the lineage, Sulfolobus turreted icosahedral virus, infecting a crenarchaeal host, has been identified in the domain Archaea. In this study we characterize the genomic sequences of two archaeal proviruses, TKV4 and MVV,integrated into the 5′- and 3′-distal regions of tRNA genes of the euryarchaeal species Thermococcus kodakaraensis KOD1 and Methanococcus voltae A3, respectively. Bioinformatic approaches allowed placement of TKV4 and MVV into the PRD1-adenovirus lineage, thus extending the lineage to the second archaeal phylum, Euryarchaeota. © 2008 Elsevier Inc. All rights reserved. Keywords: Virus evolution; Archaeal viruses; Comparative genomics; PRD1-adenovirus lineage Introduction the genes in the viruses' genomes. However, with this caveat, we have found it useful to speak of lineages of viruses in terms of the Relationships between viruses that may have a common lineages of the genes specifying virion structure. The virion- origin but diverged early in evolution cannot easily be traced by specifying genes constitute the sole part of the virus' genome standard sequence analysis techniques, which are usually only that uniquely identifies it as a virus rather than some other sort of effective for comparison of closely related entities. However, genetic element such as a plasmid. We take this part of the virus recent advances in structural analysis of viruses led to a real- as its most characteristic feature and call it the viral “self”.Itis ization that viruses considered to be unrelated, infecting thus likely that such “self” determinants are inherited vertically evolutionary distant hosts, can be unexpectedly similar (Bam- (Bamford, 2003). On the other hand, viral genes encoding ford et al., 2005a). The similarity extends from general prin- proteins involved in the interaction of a virus with its host are ciples of the virion architecture to the topology of the major likely to be transferred between unrelated viruses via lateral gene capsid proteins (MCPs). It is clear that over evolutionary time flow and, consequently, belong to the second group of viral viruses have exchanged genes and groups of genes horizontally, determinants, the “nonself” category. This category includes with the result that individual viruses are mosaics of genes with such determinants as replication, transcription regulation, different evolutionary histories. This means that it is not possible recombination, lysis, and viral entry functions (Bamford et al., to describe a lineage for viruses that applies to all or even most of 2005a; Krupovič and Bamford, 2007). Viruses sharing related “self” elements can be grouped into lineages (Bamford, 2003; Bamford et al., 2005a; Benson et al., 2004). One such viral lineage is the PRD1-adenovirus lineage, ⁎ Corresponding author. Viikki Biocenter, P.O. Box 56 (Viikinkaari 5), FIN- 00014, University of Helsinki, Finland. Fax: +358 9 191 59098. which unites icosahedral tailless viruses with dsDNA genomes. E-mail addresses: [email protected] (M. Krupovič), The core structural features of these viruses include trimeric [email protected] (D.H. Bamford). MCPs (whose subunits have a double β-barrel fold) arrayed as 0042-6822/$ - see front matter © 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.virol.2008.01.043 M. Krupovič, D.H. Bamford / Virology 375 (2008) 292–300 293 triangular plates to form the icosahedral virus coat (Bamford et al., PRD1-adenovirus lineage. Intuitively, these “self” genes are 2005a). Under the icosahedral protein shell, members of this the best seed candidates when trying to find new viruses of the lineage usually possess an internal membrane, the only exception same lineage using bioinformatic tools. This approach was known being adenovirus, which lacks lipids among its structural successfully applied to identify thirteen putative prophages components. In addition to the common MCP, members of the (viral genomes integrated into bacterial chromosome) closely PRD1-adenovirus lineage share a characteristic ATPase, exem- related to the virulent icosahedral membrane-containing bac- plified by the packaging ATPase P9 of bacteriophage PRD1 teriophage PM2 (Krupovič and Bamford, 2007). Here we used (Strömsten et al., 2005). The MCP and the ATPase seem to be the the same strategy to extend the archaeal branch of the PRD1- only two genes that are shared throughout the lineage. adenovirus lineage. The PRD1-adenovirus lineage spans all three domains of life The MCP of Sulfolobus turreted icosahedral virus (STIV) (Benson et al., 1999, 2004; Khayat et al., 2005; Nandhagopal which infects the acidophilic hyperthermophilic crenarchaeon et al., 2002). In the domain Bacteria, the lineage is represented Sulfolobus solfataricus (Rice et al., 2004) was used as a query by the phages PRD1 and PM2, which infect enterobacteria and in the PSI-BLAST search (Altschul et al., 1997). The only marine pseudoalteromonas, respectively (Benson et al., 1999; sequence that returned with a considerable E-value (1.5e-2) was Abrescia et al., submitted), and a group of Bam35-like phages, the hypothetical protein TK1353 (accession no. YP_183766) infecting Gram-positive Bacillus species (Benson et al., 2004; from T. kodakaraensis KOD1. After the second iteration a Laurinmaki et al., 2005). The eukaryotic branch of the lineage hypothetical protein (accession no. EDP40293) from M. voltae contains adenoviruses, phycodnaviruses, iridoviruses, and pos- A3 was identified (E=9e-17). sibly Mimivirus and poxviruses (Benson et al., 1999, 2004; We next verified the adjacent genomic regions of Hyun et al., 2007; Nandhagopal et al., 2002; Yan et al., 2005). T. kodakaraensis KOD1 and M. voltae A3 for the presence of The third domain of life, Archaea, is divided into two major the second “self” determinant, the putative packaging ATPase- phyla, Euryarchaeota and Crenarchaeota (Woese et al., 1990). coding gene. Indeed, in both cases open reading frames (ORFs) Only two archaeal spherical viruses, Sulfolobus turreted encoding putative ATPases were detected. Detailed analysis of icosahedral virus (STIV) and SH1, have been characterized the two putative viral regions is presented below. (Bamford et al., 2005b; Maaty et al., 2006; Porter et al., 2005; Rice et al., 2004). STIV infects a crenarchaeal host, while SH1 is Integration sites of putative proviruses TKV4 and MVV a halovirus infecting the euryarchaeon Haloarcula hispanica. Both virions possess an internal membrane covered by an Archaeal integrases can be divided into two types based on the icosahedral capsid (Bamford et al., 2005b; Maaty et al., 2006) integration mechanisms (She et al., 2004). A characteristic of the and therefore share general features common to the majority of first type (SSV1-type) integrases is that, upon integration of the the PRD1-adenovirus lineage members. While the high-resolu- circular genetic element (virus genome or plasmid) into the host tion structure of the MCP of STIV confirmed that it is a genuine chromosome, the integrase gene is partitioned into longer Int (C) member of the lineage (Khayat et al., 2005), recent structural and shorter Int (N) fragments. The second type is comprised of analysis of the SH1 virion by electron microscopy revealed that it enzymes that maintain an intact integrase-coding gene after has a novel capsid arrangement, distinct from the canonical one integration. In both cases, the att sites are usually highly similar seen in members of the PRD1-adenovirus lineage (Jäälinoja or identical to the 3′-distal regions of a tRNA gene, which is et al., submitted for publication). Therefore, the question of therefore used as the integration site (Reiter et al., 1989). For type whether the PRD1-adenovirus lineage can be extended to the I integrases the att site is located inside the viral integrase gene, phylum Euryarchaeota in the domain Archaea remains open. while those for type II are adjacent to the integrase gene (She Various parasitic elements, such as viruses and transposable et al., 2004). Upon integration of the circular genetic element, the elements, usually constitute a considerable fraction of cellular att sequence flanks the inserted element as a direct repeat. genomes. Therefore, genome analysis of a cellular organism T. kodakaraensis KOD1 is a hyperthermophilic euryarch- provides information not only on the organism itself, but might aeon isolated from a solfatara
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